Antimicrobial resistance and transmission potential of pet-derived Providencia spp. in China

• First detection of P. hangzhouensis in a canine urinary tract infection. • P. hangzhouensis showed expanded β-lactam and fluoroquinolone resistance . • The ESBL gene bla PER-1 and gyrA/parC mutations occurred in specific isolates. • A novel plasmidborne IS 26 -flanked composite transposon carrying tetR(D) and tet (D) was identified. • Pet-derived Providencia isolates were phylogenetically linked to human and environmental isolates. Providencia spp. are opportunistic Gram-negative pathogens associated with urinary tract, wound, and healthcare-associated infections. Although reported in livestock, little is known about the occurrence and AMR of Providencia spp. in pets. This study aimed to investigate the prevalence, antimicrobial resistance profiles, and genomic characteristics of Providencia spp. isolated from diseased pets in China. Overall, 7,633 canine and feline clinical isolates collected between 2018 and 2023 were screened for Providencia spp.. Antimicrobial susceptibility testing, whole-genome sequencing, plasmid analysis, and phylogenetic analysis were performed to characterize resistance determinants and assess potential transmission relationships. Six Providencia isolates from dogs were identified: five Providencia stuartii and, for the first time in pets, one Providencia hangzhouensis . The P. stuartii isolates exhibited resistance to fluoroquinolones, florfenicol, and trimethoprim-sulfamethoxazole, while remaining largely susceptible to 3 rd and 4 th generation cephalosporins and carbapenems. In contrast, the P. hangzhouensis isolate (23p6) showed resistance to cephalosporins. Whole-genome sequencing revealed multiple resistance and virulence genes, as well as mutations in gyrA and parC associated with fluoroquinolone resistance. Plasmid analysis identified an IS 26 -flanked composite transposon carrying tet (D) in close proximity to bla TEM-1 . Phylogenetic analysis demonstrated close relatedness between pet-derived P. stuartii isolates and human and environmental isolates, while the P. hangzhouensis isolate clustered with fly-derived isolates, suggesting potential cross-species and environmental transmission. This study expands the host spectrum of Providencia spp. and provides the first evidence of P. hangzhouensis in companion animals, highlighting their potential role in AMR dissemination and the need for enhanced surveillance and prudent antimicrobial use.